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Octopus Genome Defies Evolutionary Expectations


Cephalopods, from the Latin for "head-foot," are among the strangest creatures in the ocean. Though classified in phylum Mollusca, they seem vastly different from snails or clams. Colorful octopus and cuttlefish swim by in the introduction to Living Waters: Intelligent Design in the Oceans of the Earth, but it would require whole separate films to do them justice -- for they are among the smartest and most functionally diverse animals on the planet: flexible, adaptable, and well-equipped for rapid motion, effective hunting, and quick camouflage.

Their numbers include the giant squid, cuttlefish, and the beautifully coiled shelled nautilus. Now that the first octopus genome has been sequenced, scientists are beginning to learn about the complex genetic information behind their capabilities.

Nature published the first genome of a cephalopod, the California two-spot octopus, Octopus bimaculoides. It was a massive undertaking. The octopus genome is comparable to the human genome in size and complexity. In fact, it has "a greater number of protein-coding genes -- some 33,000, compared with fewer than 25,000 in Homo sapiens," says Alison Abbott in the same issue of Nature.

This excess results mostly from the expansion of a few specific gene families, Ragsdale says. One of the most remarkable gene groups is the protocadherins, which regulate the development of neurons and the short-range interactions between them. The octopus has 168 of these genes -- more than twice as many as mammals. This resonates with the creature's unusually large brain and the organ's even-stranger anatomy. Of the octopus's half a billion neurons -- six times the number in a mouse -- two-thirds spill out from its head through its arms, without the involvement of long-range fibres such as those in vertebrate spinal cords. The independent computing power of the arms, which can execute cognitive tasks even when dismembered, have made octopuses an object of study for neurobiologists such as Hochner and for roboticists who are collaborating on the development of soft, flexible robots.

A gene family that is involved in development, the zinc-finger transcription factors, is also highly expanded in octopuses. At around 1,800 genes, it is the second-largest gene family to be discovered in an animal, after the elephant's 2,000 olfactory-receptor genes. [Emphasis added.]

Is this an example of the power of Darwinian evolution to progressively expand existing traits? Don't ask the geneticists; they're too busy trying to figure out where all the unique genes came from.

The analysis also turned up hundreds of other genes that are specific to the octopus and highly expressed in particular tissues. The suckers, for example, express a curious set of genes that are similar to those that encode receptors for the neurotransmitter acetylcholine. The genes seem to enable the octopus's remarkable ability to taste with its suckers.

Scientists identified six genes for proteins called reflectins, which are expressed in an octopus's skin. These alter the way light reflects from the octopus, giving the appearance of a different colour -- one of several ways that an octopus can disguise itself, along with changing its texture, pattern or brightness.

Another discovery hinted at the basis of an octopus's intelligence. The genome contains systems that can allow tissues to rapidly modify proteins to change their function. Electrophysiologists had predicted that this could explain how octopuses adapt their neural-network properties to enable such extraordinary learning and memory capabilities.

How could so many unique genes arise by blind neo-Darwinian processes? It's unsatisfying to hear scientists assume they "developed" somehow.

The octopus's position in the Mollusca phylum illustrates evolution at its most spectacular, Hochner says. "Very simple molluscs like the clam -- they just sit in the mud, filtering food. And then we have the magnificent octopus, which left its shell and developed the most-elaborate behaviours in water."

The paper is no help. It just speaks of "cephalopod morphological innovations, including their large and complex nervous systems." And then, the authors find they cannot appeal to a favorite explanatory tool, gene duplication:

Based primarily on chromosome number, several researchers proposed that whole-genome duplications were important in the evolution of the cephalopod body plan, paralleling the role ascribed to the independent whole-genome duplication events that occurred early in vertebrate evolution. Although this is an attractive framework for both gene family expansion and increased regulatory complexity across multiple genes, we found no evidence for it. The gene family expansions present in octopus are predominantly organized in clusters along the genome, rather than distributed in doubly conserved synteny as expected for a paleopolyploid.... Although genes that regulate development are often retained in multiple copies after paleopolyploidy in other lineages, they are not generally expanded in octopus relative to limpet, oyster and other invertebrate bilaterians.

With whole-genome duplication out, what's left? Essentially, magic:

Mechanisms other than whole-genome duplications can drive genomic novelty, including expansion of existing gene families, evolution of novel genes, modification of gene regulatory networks, and reorganization of the genome through transposon activity. Within the O. bimaculoides genome, we found evidence for all of these mechanisms, including expansions in several gene families, a suite of octopus- and cephalopod-specific genes, and extensive genome shuffling.

"Evolution of novel genes" --? Isn't that the question at hand? Where do novel genes come from? They found "a suite of octopus- and cephalopod-specific genes" that seem to have appeared out of nowhere. As for mechanisms that "can drive genomic novelty," their list does little more than assume that making more of existing things and shuffling them around will create novel things that do something useful. Try that with a copy machine, a book, and scissors. "Modification of gene regulatory networks" is no help, either. Stephen Meyer documented in Darwin's Doubt how modifications to GRNs are almost always lethal, and never innovative.

Running out of options, the authors turn to a perennial cop-out: convergence.

A search of available transcriptome data from the longfin inshore squid Doryteuthis (formerly, Loligo) pealei also demonstrated an expanded number of protocadherin genes... Surprisingly, our phylogenetic analyses suggest that the squid and octopus protocadherin arrays arose independently. Unlinked octopus protocadherins appear to have expanded ~135 Mya, after octopuses diverged from squid. In contrast, clustered octopus protocadherins are much more similar in sequence, either due to more recent duplications or gene conversion as found in clustered protocadherins in zebrafish and mammals....

Finally, the independent expansions and nervous system enrichment of protocadherins in coleoid cephalopods and vertebrates offers a striking example of convergent evolution between these clades at the molecular level.

Maybe octopus evolved from fish into mammals. We jest, of course, but the genomic data are not proving helpful to Darwin. After comparing the genome to other creatures near and far, finding more examples of unique genes and convergences, the authors close by trying to put the octopus in context with the family tree of lophotrochozoans ("crest-wheel" animals, a controversial supergroup of phyla that includes animals as diverse as worms, clams, and brachiopods). Watch again for the magical appearance of innovations:

Using a relaxed molecular clock, we estimate that the octopus and squid lineages diverged ~270 Mya, emphasizing the deep evolutionary history of coleoid cephalopods... Our analyses found hundreds of coleoid- and octopus-specific genes, many of which were expressed in tissues containing novel structures, including the chromatophore-laden skin, the suckers and the nervous system.... Taken together, these novel genes, the expansion of C2H2 ZNFs, genome rearrangements, and extensive transposable element activity yield a new landscape for both trans- and cis-regulatory elements in the octopus genome, resulting in changes in an otherwise 'typical' lophotrochozoan gene complement that contributed to the evolution of cephalopod neural complexity and morphological innovations.

Maybe this is why Alison Abbott jokes about the octopus having the genome of an alien. "With its eight prehensile arms lined with suckers, camera-like eyes, elaborate repertoire of camouflage tricks and spooky intelligence, the octopus is like no other creature on Earth."

Over at Science, Dennis Normile has nothing new to offer. The octopus genome "surprises and teases," he says. He quotes a team member from the University of Chicago who speaks for the team: "We were really pretty surprised by a bunch of things we found." Another researcher offers this unhelpful comment on the implications for evolution: "there is more than one way to grow a genome."

The popular media took all these surprises in stride, never doubting Darwin, but having little to say about him, either. Most pointed out that the genome-duplication trick doesn't work for the octopus. Discussion of evolution is remarkably scarce in the articles. One exception is Science Daily. Its write-up not only credits blind nature for all the octopus's innovations, but launches into a victory speech for cosmic Darwinism:

As humans, we like to think we are unique in evolutionary terms, but the octopus could reveal that this is not the case. One reason the octopus fascinates scientists is that its brain became organized to be able to carry out such incredible, complex tasks without adopting the principles of the vertebrate brain. Further examination will tell if the building blocks of its nervous system are as radically different from those of vertebrate landlubbers like us, as the octopus's abilities suggest.

This is not as unlikely as it sounds. Even if the octopus evolved in a completely different ecosystem, evolution can have only so many solutions to a given problem. If similarities are in fact found, this would significantly alter our perspective on the emergence of life elsewhere in the universe.

David Klinghoffer has pointed out how off-putting triumphalism like this can be. Can't reporters just be honest about the problems with traditional evolutionary explanations? In Living Waters, Discovery Institute's Richard Sternberg and Paul Nelson discuss how improbable it is to get two coordinated mutations for a new function. For the case of whale evolution, the time required for just two mutations for some adaptation vastly exceeds the time available for the transition. A similar problem is evident with octopus evolution from a "simple" mollusk.

Science can observe and enjoy wonders of nature without a Darwinian narrative gloss. Though Live Science's coverage of the Nature paper was heavy on the gloss, a different Live Science article described another species, the large Pacific striped octopus (LPSO), with whimsical delight and very little talk about evolution. This species (despite its name, able to compact itself the size of a tennis ball), tricks its prey the way a human jokester taps on a friend's opposite shoulder, making him turn the wrong way.

"One of the things that impresses me most about this species is its great diversity of predatory behavior," Caldwell told Live Science. Not only does this striped octopus trick unsuspecting shrimp, but it also eats snails by first boring small holes into their shells with the end of its arm and then injecting its prey with a deadly, digestive fluid, he said. And despite their diminutive size, LPSOs are strong enough to break apart a clam shell and spritely enough to pounce on a quick-footed crab.

But the extraordinary eating habits of this critter don't end there. Once an LPSO catches its supper, it isn't above sharing the meal with others, said Caldwell, who notes that the animal's ability to peacefully share food with other octopuses is both unusual and very exciting to biologists.

Scientific investigation can still be "very exciting" without the Darwinian angle. There are many more species of cephalopods worth investigating. Some live deep at hydrothermal vents. Some live in shallow tide pools. They come in all sizes. The mimic octopus amazes scientists. There is much to occupy biologists' time learning about these wonderful animals, without having to fit them into an evolutionary tree.

"There are over 300 known species of octopus, and more are described every year. But the fact is that while we think we know a lot about octopus behavior and physiology, everything we know comes from a handful of species," Caldwell said. "So when I tell you the LPSO is an unusual species with very unique behavior, I really don't know that."

Meanwhile, several of the articles mention that engineers are studying octopuses in search of ideas for soft robots, distributed networks, and propulsion techniques. "Humans invented flying machines by mimicking birds," Science Daily says. "We can look forward to octopuses inspiring robots that give us easy access to the ocean floor."

It's unlikely to be productive trying to trace an assumed evolutionary ancestry that requires heavy doses of "innovation" or "convergence" to accept. Why not tackle the questions amenable to observation and understanding? Biomimetics is showing the usefulness of a design approach. Let's follow that evidence where it leads.

Image: Octopus bimaculoides, by Jeremyse at en.wikipedia [Public domain], via Wikimedia Commons.